Starvation reveals the cause of infection-induced castration and gigantism.

Cressler CE, Nelson WA, Day T, McCauley E - Proc. Biol. Sci. (2014)

Bottom Line:
Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them.Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration.These results are consistent with an energetic structure where the parasite uses growth energy as a resource.

ABSTRACTParasites often induce life-history changes in their hosts. In many cases, these infection-induced life-history changes are driven by changes in the pattern of energy allocation and utilization within the host. Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them. Determining the causes and consequences of infection-induced life-history changes requires the ability to experimentally manipulate life history and a framework for connecting life history to host and parasite fitness. Here, we combine a novel starvation manipulation with energy budget models to provide new insights into castration and gigantism in the Daphnia magna-Pasteuria ramosa host-parasite system. Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration. These results are consistent with an energetic structure where the parasite uses growth energy as a resource. This finding gives us new understanding of the role of castration and gigantism in this system, and how life-history variation will affect infection outcome and epidemiological dynamics. The approach of combining targeted life-history manipulations with energy budget models can be adapted to understand life-history changes in other disease systems.

RSPB20141087F1: Predicted host and parasite response to changing energy flow to host reproduction. (a) Alternative energy budget models for parasite growth in the D. magna–P. ramosa system. These models are based on the dynamic energy budget framework of [16]. F is food in the environment; E is energy reserves, a temporary storage buffer for assimilated energy; S is somatic tissue; R is reproductive investment; and P is the parasite population. In all models, infection causes energy to be reallocated from reproduction to growth, as indicated by the dashed arrows. Model 1 posits that parasites use the reserves as a resource [15], model 2 posits that parasites use growth allocation as a resource [11] and model 3 posits the parasites use reproduction allocation as a resource, with any surplus reallocated to growth. (b–d) Responses of host life history and parasite fitness to an experimental treatment that changes the energy flowing to reproduction without affecting the energy to growth. (b) In all models, increasing the energy to reproduction increases host size. (c) Models 1 and 2 predict no response of age at castration to the treatment, whereas model 3 predicts a more rapid onset of castration. (d) Model 1 predicts no response of parasite fitness to treatment, whereas models 2 and 3 predict that parasite fitness will increase. The label Td denotes the feeding interval in days (d) used to manipulate host reproduction.

Mentions:
Previous authors have proposed proximate energetic explanations for how castration and gigantism arise in infected individuals [8,11], but there are several ways this could occur, and model predictions have never been directly compared against one another or against empirical data. Figure 1a shows three heuristic energy budget model structures for this system. These models are based on the framework of dynamic energy budget theory [12] and share broad similarities. In particular, under all models, castration and gigantism benefit the parasite [8,21]. Following castration, energy not captured by the parasite goes into host growth. The timing of castration is hypothesized to depend on the parasite's population growth rate (prior to castration). This is because castration is likely to be hormonal [8,14]; if hormone production is density-dependent, then castration occurs when the parasite population reaches some critical size [11]. The critical distinction among the models is in their assumption about where, in the normal host energy budget, the parasite gets its energy. Thus, comparing model-predicted responses to an experimental perturbation of energetics against empirical data can reveal which model structure is most appropriate for this system. In particular, consider an experimental treatment that holds total resource ingestion constant but reduces the amount of energy going to reproduction without affecting the amount of energy going to growth. The models predict very different responses of host gigantism, timing of castration and lifetime parasite fitness to such a treatment (figure 1b–d).Figure 1.

RSPB20141087F1: Predicted host and parasite response to changing energy flow to host reproduction. (a) Alternative energy budget models for parasite growth in the D. magna–P. ramosa system. These models are based on the dynamic energy budget framework of [16]. F is food in the environment; E is energy reserves, a temporary storage buffer for assimilated energy; S is somatic tissue; R is reproductive investment; and P is the parasite population. In all models, infection causes energy to be reallocated from reproduction to growth, as indicated by the dashed arrows. Model 1 posits that parasites use the reserves as a resource [15], model 2 posits that parasites use growth allocation as a resource [11] and model 3 posits the parasites use reproduction allocation as a resource, with any surplus reallocated to growth. (b–d) Responses of host life history and parasite fitness to an experimental treatment that changes the energy flowing to reproduction without affecting the energy to growth. (b) In all models, increasing the energy to reproduction increases host size. (c) Models 1 and 2 predict no response of age at castration to the treatment, whereas model 3 predicts a more rapid onset of castration. (d) Model 1 predicts no response of parasite fitness to treatment, whereas models 2 and 3 predict that parasite fitness will increase. The label Td denotes the feeding interval in days (d) used to manipulate host reproduction.

Mentions:
Previous authors have proposed proximate energetic explanations for how castration and gigantism arise in infected individuals [8,11], but there are several ways this could occur, and model predictions have never been directly compared against one another or against empirical data. Figure 1a shows three heuristic energy budget model structures for this system. These models are based on the framework of dynamic energy budget theory [12] and share broad similarities. In particular, under all models, castration and gigantism benefit the parasite [8,21]. Following castration, energy not captured by the parasite goes into host growth. The timing of castration is hypothesized to depend on the parasite's population growth rate (prior to castration). This is because castration is likely to be hormonal [8,14]; if hormone production is density-dependent, then castration occurs when the parasite population reaches some critical size [11]. The critical distinction among the models is in their assumption about where, in the normal host energy budget, the parasite gets its energy. Thus, comparing model-predicted responses to an experimental perturbation of energetics against empirical data can reveal which model structure is most appropriate for this system. In particular, consider an experimental treatment that holds total resource ingestion constant but reduces the amount of energy going to reproduction without affecting the amount of energy going to growth. The models predict very different responses of host gigantism, timing of castration and lifetime parasite fitness to such a treatment (figure 1b–d).Figure 1.

Bottom Line:
Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them.Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration.These results are consistent with an energetic structure where the parasite uses growth energy as a resource.

ABSTRACTParasites often induce life-history changes in their hosts. In many cases, these infection-induced life-history changes are driven by changes in the pattern of energy allocation and utilization within the host. Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them. Determining the causes and consequences of infection-induced life-history changes requires the ability to experimentally manipulate life history and a framework for connecting life history to host and parasite fitness. Here, we combine a novel starvation manipulation with energy budget models to provide new insights into castration and gigantism in the Daphnia magna-Pasteuria ramosa host-parasite system. Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration. These results are consistent with an energetic structure where the parasite uses growth energy as a resource. This finding gives us new understanding of the role of castration and gigantism in this system, and how life-history variation will affect infection outcome and epidemiological dynamics. The approach of combining targeted life-history manipulations with energy budget models can be adapted to understand life-history changes in other disease systems.